Mi-1-Mediated Aphid Resistance Involves Salicylic Acid and Mitogen-Activated Protein Kinase Signaling Cascades

Abstract

The tomato Mi-1 gene confers resistance to root-knot nematodes (Meloidogyne spp.), potato aphids (Macrosiphum eluphorbiae), and whiteflies (Bemisia tabaci and B. tabaci biotype B). Resistance to potato aphid is developmentally regulated and is not associated with induction of a hypersensitive response. The NahG transgene that eliminates endogenous salicylic acid (SA) was used to test the role of the SA signaling pathway in the resistance mediated by Mi-1 to potato aphids. Aphids survived longer on NahG tomato plants than on wild type. However, aphid reproduction was not affected on NahG tomato. Aphid resistance in Mi-1 NahG plants was completely abolished and the phenotype was successfully rescued by application of BTH (benzo(1,2,3)-thiaiazole-7-carbothioic acid S-methyl ester), indicating that the SA signaling pathway is an important component of Mi-1-mediated aphid resistance. Using virus-induced gene silencing, one or more mitogen-activated protein kinase (MAPK) cascades required for Mi-1-mediated aphid resistance were identified. Silencing plants for MAPK kinase (LeMKK2) and MAPKs (LeMPK2 and LeMPK1, or LeMPK3) resulted in attenuation of Mi-1-mediated aphid resistance. These results further demonstrate that resistance gene-mediated signaling events against piercing-sucking insects are similar to those against other plant pathogens.

Tomato MAPKs LeMPK1, LeMPK2, and LeMPK3 function in the systemin-mediated defense response against herbivorous insects

“…LeMPK1/2/3 had been shown to function in host-specific AvrPto-dependent resistance to the bacterial pathogen P. syringae (28,45) and in Mi-1-mediated resistance to aphids (29). Our reduction-of-function study demonstrates that LeMPK1 and LeMPK2 are required for systemin-mediated resistance to M. sexta larvae.…”

“…Loss-of-function studies had shown they are required for defense against P. syringae and Mi-1-mediated resistance to aphids (29). In this study, we used virus-induced gene silencing (VIGS) and showed that these LeMPKs also function upstream of JA and are required for expression of a subset of wound-response genes and resistance to herbivorous insects.…”

The Coiled-Coil and Nucleotide Binding Domains of BROWN PLANTHOPPER RESISTANCE14 Function in Signaling and Resistance against Planthopper in Rice

“…SA and JA are well-established plant signaling molecules that mediate defense responses to insects (Walling, 2000;Li et al, 2006;Zarate et al, 2007;Du et al, 2009;Browse, 2009;Zhao et al, 2016). The transcript levels of SA biosynthesis-related genes accumulated more rapidly and were maintained at higher levels in CC and NB transgenic plants than in wild-type plants.…”

Resistance-Gene-Mediated Defense Responses against Biotic Stresses in the Crop Model Plant Tomato

“…By applying VIGS in tomato plants it has been shown that Mi-1.2-mediated resistance against nematodes and aphids requires Hsp90, Sgt1, members of the MAP kinase cascade and WRKY transcription factors (Figure 1) [138][139][140][141]. In addition, by utilizing transgenic tomato plants expressing NahG (encodes for an enzyme that metabolizes SA) a role for SA in Mi-1-mediated resistance to potato aphids was identified [141].…”

“…In a genetic based screening F2 tomato seedlings, those homozygous for the eds1 mutation (eds1/eds1) and those that were heterozygous (EDS1/eds1), were chosen for a disease assay and were inoculated with Fol race 3. Samples were screened for the disease resistance and it was found that EDS1 is required for I-7 mediated resistance [53].By applying VIGS in tomato plants it has been shown that Mi-1.2-mediated resistance against nematodes and aphids requires Hsp90, Sgt1, members of the MAP kinase cascade and WRKY transcription factors (Figure 1) [138][139][140][141]. In addition, by utilizing transgenic tomato plants expressing NahG (encodes for an enzyme that metabolizes SA) a role for SA in Mi-1-mediated resistance to potato aphids was identified [141].…”